The cisproline(i-1)-aromatic(i) interaction: Folding of the Ala-cisPro-Tyr peptide characterized by NMR and theoretical approaches

Frederico Nardi, Johan Kemmink, Michael Sattler, Rebecca C. Wade

European Molecular Biology Laboratory, Postfach 10.2209, Meyerhofstrae 1, D-69012 Heidelberg, Germany


Abstract
proline( i -1) - aromatic( i ) interactions have been detected in several short peptides in aqueous solution by analysis of anomalous chemical shifts measured by 1H-NMR spectroscopy. This formation of local structure is of importance for protein folding and binding properties. To obtain an atomic - detail characterisation of the cisproline( i -1) - aromatic( i ) interaction in terms of structure, energetics and dynamics, we studied the minimal peptide unit, blocked Ala - cisPro - Tyr, using computational and experimental techniques. Structural database analyses and a systematic search revealed two groups of conformations displaying a cisproline( i -1) - aromatic( i ) interaction. These conformations were taken as seeds for molecular dynamics simulations in explicit solvent at 278 K. During a total of 33.6 ns of simulation, all the 'folded' conformations and some `unfolded' states were sampled. 1H- and 13C-chemical shifts and 3J-coupling constants were measured for the Ala-Pro-Tyr peptide. Excellent agreement was found between all the measured and computed NMR properties, showing the good quality of the force field. We find that under the experimental and simulation conditions, the Ala - cisPro - Tyr peptide is folded 90% of the time and displays two types of folded conformation which we denote 'a' and 'b'. The type a conformations are twice as populated as the type b conformations. The former have the tyrosine ring interacting with the alanine alpha proton and are enthalpically stabilised. The latter have the aromatic ring interacting with the proline side chain and are entropically stabilised. The combined and complementary use of computational and experimental techniques permitted derivation of a detailed scenario of the 'folding' of this peptide.


Keywords
chemical shift, cisproline - aromatic interaction, conformational search, molecular dynamics, peptide folding in aqueous solution


Journal of Biomolecular NMR 17 (1): 63-77, May 2000
Kluwer Academic Publishers
Article ID: 266528


Supplementary Material Privacy Imprint